Recurrent co-domestication of PIF/Harbinger transposable element proteins in insects

BACKGROUND: Transposable elements (TEs) are selfish DNA sequences capable of moving and amplifying at the expense of host cells. Despite this, an increasing number of studies have revealed that TE proteins are important contributors to the emergence of novel host proteins through molecular domestication. We previously described seven transposase-derived domesticated genes from the PIF/Harbinger DNA family of TEs in Drosophila and a co-domestication. All PIF TEs known in plants and animals distinguish themselves from other DNA transposons by the presence of two genes. We hypothesize that there should often be co-domestications of the two genes from the same TE because the transposase (gene 1) has been described to be translocated to the nucleus by the MADF protein (gene 2). To provide support for this model of new gene origination, we investigated available insect species genomes for additional evidence of PIF TE domestication events and explored the co-domestication of the MADF protein from the same TE insertion. RESULTS: After the extensive insect species genomes exploration of hits to PIF transposases and analyses of their context and evolution, we present evidence of at least six independent PIF transposable elements proteins domestication events in insects: two co-domestications of both transposase and MADF proteins in Anopheles (Diptera), one transposase-only domestication event and one co-domestication in butterflies and moths (Lepidoptera), and two transposases-only domestication events in cockroaches (Blattodea). The predicted nuclear localization signals for many of those proteins and dicistronic transcription in some instances support the functional associations of co-domesticated transposase and MADF proteins. CONCLUSIONS: Our results add to a co-domestication that we previously described in fruit fly genomes and support that new gene origination through domestication of a PIF transposase is frequently accompanied by the co-domestication of a cognate MADF protein in insects, potentially for regulatory functions. We propose a detailed model that predicts that PIF TE protein co-domestication should often occur from the same PIF TE insertion. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13100-022-00282-2.